Adolescent idiopathic scoliosis, bracing, and the Hueter-Volkmann principle

The Spine Journal 3 (2003) 180–185

Clinical Studies

Adolescent idiopathic scoliosis, bracing, and the Hueter-Volkmann principle Frank P. Castro, Jr., MD* Spine Surgery, PSC, 210 East Gray Street, Suite 601, Louisville, KY 40202, USA Received 12 February 2002; accepted 18 September 2002

Abstract

Background context: Evidence demonstrating the biomechanical effects of the Hueter-Volkmann principle on vertebral body growth in spinal deformities is lacking. Bracing a scoliotic curve should, in theory, unload the growth plates on the concave side of the vertebral bodies near the curve’s apex. Growth stimulation, leading to structural remodeling of the vertebral bodies, on the curve’s concave side may explain the improvement or lack of curve progression, as measured by Cobb angles, reported with successful brace management of adolescent idiopathic scoliosis (AIS). Purpose: To determine whether brace treatment stimulated asymmetric chondrogenesis in the apical three vertebral bodies. Study design: A prospective cohort of patients with AIS receiving brace treatment were followed from the initiation of brace treatment until skeletal maturity. Patients were then retrospectively divided into those with and without radiographic progression. This post hoc analysis was included to determine risk factors for curve progression. Patient sample: Forty-one skeletally immature patients with AIS meeting criteria for brace treatment were followed until skeletal maturity. All patients were treated with thoracolumbosacral orthotics (TLSOs). Outcome measures: The positional derotation of the TLSO on the spine was measured by comparing the initial radiograph with the first radiograph in a brace. The long-term structural changes of the vertebral bodies were determined by comparing the initial and final radiographs. Differences in initial radiographic parameters between the groups of patients with AIS with and without curve progression indicated predictive factors for successful brace treatment. Methods: Initial radiographic measurements were compared with those observed in a brace and those observed at final follow-up. The same analysis was retrospectively repeated comparing patients with AIS with and without radiographic progression. Results: Cobb measurements (p.0001) and concave-to-convex height ratios of the apical three vertebral bodies improved when the brace was initially applied (p.0035). Structural remodeling or a rotational correction of the apical three vertebral bodies was appreciated only in patients with flexible curves (p.01). Conclusion: Brace application results in immediate positional derotations of the spine in patients with AIS. These positional derotations were maintained only in patients with flexible curves, at final follow-up. Brace treatment was not recommended in patients whose curves did not correct at least 20% in a TLSO. © 2003 Elsevier Inc. All rights reserved.

Keywords:

Scoliosis; Hueter-Volkmann; Remodeling; Growth; Bracing

FDA device/drug status: not applicable. Nothing of value received from a commercial entity related to this research. * Corresponding author. Spine Surgery, PSC, 210 East Gray Street, Suite 601, Louisville, KY 40202, USA. Tel.: (502) 585-2300; fax (502) 584-2726. E-mail address: http://www.spine-surgery.com 1529-9430/03/$ – see front matter © 2003 Elsevier Inc. All rights reserved. PII: S1529-9430(02)005 5 7 - 0

F.P. Castro et al. / The Spine Journal 3 (2003) 180–185

Introduction Bracing is the primary nonoperative treatment for skeletally immature adolescents with idiopathic scoliosis [1–4]. The generally accepted guidelines include all curves with documented progression in the coronal plane of greater than 10 degrees or curves with Cobb angles between 20 and 40 degrees [2,5–7]. Controversies exist over the number of hours the brace must be worn [8–11], the type of brace [8,11], the tension of the straps [12], the role of vestibular dysfunction [13], the interaction of hormones [14,15] and the efficacy of bracing [1,5,16]. Several authors believe that the Hueter-Volkmann principle contributes to the development of adolescent idiopathic scoliosis (AIS) [15,17–21]. Briefly stated, asymmetric loading or compression of the growth plates on the concave side of the curve(s) inhibit growth leading to wedging of the vertebral bodies. Bracing a scoliotic curve should, in theory, unload the growth plates on the concave side of the vertebral bodies near the curve’s apex. Growth stimulation, leading to structural remodeling of the vertebral bodies, on the curve’s concave side may explain the improvement or lack of curve progression, as measured by Cobb angles, reported with successful brace management of AIS [3–5]. Evidence demonstrating the biomechanical effects of the Hueter-Volkmann principle on vertebral body growth in spinal deformities is lacking. To our knowledge, no longitudinal study of the Hueter-Volkmann principle and vertebral body growth rate in patients with AIS has been published. The threshold and limit of the force magnitudes necessary for the Hueter-Volkmann principle to apply in AIS have not been delineated. Because the spine simultaneously experiences compressive and tensile forces, it is unlikely that all compressive forces inhibit growth and all tensile forces stimulate growth. The purpose of this investigation was to determine whether long-term brace treatment stimulated asymmetric chondrogenesis in the apical three vertebrae. Under the null hypothesis of no effect, we made the following assumptions: 1) normal symmetric growth of the vertebral bodies, in the coronal plane, existed before the development of AIS; 2) scoliotic curves were the result of abnormal positioning of normal vertebral bodies; 3) brace application repositions the vertebral bodies into a more anatomic position and 4) the Hueter-Volkman principle applies to growth plates in patients with AIS. That is, brace treatment should accelerate chondrogenesis on the concave side of a scoliotic curve. Methods This study was conducted at the Scottish Rite Medical Center in Atlanta, Georgia. Patients with AIS were identified with the following inclusion criteria: skeletal immaturity (Risser 0 or 1) at initial presentation, a major curve between 20 and 40 degrees, treatment consisting of a thoracolumbosacral orthosis (TLSO), a

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minimum of 2 years of follow-up and documented skeletal maturity at final follow-up (Risser 5). All cases were classified according to the King classification [22] and Risser stage [23]. Although peak height velocity may have been a better indicator of skeletal (im)maturity and risk of curve progression [24], this information was not obtainable from the charts reviewed. Although numerous standing anteroposterior radiographs were made, only three radiographs were used for the statistical analysis. The first radiograph identified the patient as a brace candidate. The criteria described above were used to determine brace candidacy. In order to reflect the maximum effect of brace application, we specifically chose the standing in-brace radiograph with the best coronal plane correction in Cobb measurement. Without exception, the greatest correction in Cobb measurement was seen at the time of initial brace application. This standing in-brace radiograph occurred within 6 weeks of the first radiograph. The third radiograph used in this study was taken at the time of last follow-up. Patients were skeletally mature (Risser 5) and had been weaned out of their brace for at least 6 months. The heights of the concave and convex sides of the vertebral body above the apex, the apical vertebrae and the vertebral body below the apex were measured. A ratio was then calculated by dividing the concave side height measurement by the convex side height measurement. This ratio obviated the measurement differences caused by different target distances, object to film distances and magnification factors. The ratios would also be comparable over time. Values less than 1.0 indicated wedging of a vertebral body. Improvement in the concave-to-convex height ratio between the initial out-of-brace (first) and initial in-brace (second) radiographs would reflect brace-induced positional changes of the vertebral bodies. The comparison between the initial and final radiographs may determine the relative growth of the concave and convex sides over the study interval. This comparison may also reflect positional derotations maintained until skeletal maturity. Structural changes of the vertebral bodies consistent with asymmetric chondrogenesis and the Hueter-Volkmann principle would be implied if the concave-to-convex height ratios of the third radiographs were significantly different from those of the first radiographs and independent of any changes in the Cobb measurement. Reduction of the Cobb angle on coronal radiographs has been associated with a reduction in the rotation of the apical vertebrae [25–28]. The positive correlation between Cobb measurement and apical rotation may be explained by the coupling of rotation and translation in spinal motion segments [29]. We did not analyze rotational measurements of the apical three vertebral bodies for four reasons: 1) radiographic measurements of vertebral body rotation are notoriously inaccurate and statistically unreliable [6,29–33]; 2) the greatest correction in rotation, with distractive forces applied, usually occurs at the ends of the curve rather than at the apex [5,17,34]; 3) sagittal plane correction under distractive forces is less predictable and independent of coro-

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nal plane correction [6,34] and 4) analysis of statistically invalid variables dilutes the impact of other comparisons. Descriptive statistics were used to describe the frequency and progression of the different King curve types. The curve types were collected to document demographic similarities between the current study group and those patients with AIS receiving brace treatment previously reported in the literature. A matched pairs t test comparing the initial two radiographs was used to determine the positional effects of brace treatment. A second matched pairs t test between the initial and final radiographs was used to determine the long-term effect of brace treatment on growth of the vertebral bodies. Because two hypotheses were being tested, statistical significance was considered achieved when the p value was less than .025 (.05/2). A retrospective analysis was conducted to compare the 21 patients who demonstrated five or more Cobb degrees (Group A) with the 20 patients with AIS with no radiographic progression (Group B). The initial Cobb measurements and concave-to-convex height ratios were compared by unpaired t tests to ensure no prebrace bias. The same intragroup analyses done in the prospective analysis were repeated in the retrospective analysis. An unpaired t test comparing the difference in brace effect (Cobb measurement of the initial radiograph minus the Cobb measurement in a brace) between Groups A and B was also done. The differences in the average final vertebral body shape between Groups A and B were also compared by an unpaired t test. Results Three male and 38 female patients met inclusion criteria for the study. The average age at presentation was 12.13 months. Five patients had a King Type I curve, 16 had a King Type II curve, 11 had a King Type III curve, four had a King Type IV curve, and five had a King Type V curve. The average Cobb angle of the major curve was 280.9 degrees (Table 1). The average concave-to-convex height ratios for the vertebral body, one above the apex, the apical vertebral body and the vertebral body one below, at initial

Table 1 Demographic characteristics of the study group n

presentation were 0.910.01, 0.850.02 and 0.910.01, respectively. A statistically significant radiographic improvement of 50% was seen in the major curves’ average Cobb angle when the brace was applied (28 to 14 degrees; p.0001). The concave-to-convex height ratios also showed statistically significant improvements (p.0035). The concave-toconvex height ratios of the cephalad, apical and caudad vertebrae were 0.930.01, 0.880.01 and 0.920.01 (Table 2), respectively. Patients were encouraged to wear the braces for 23 hours a day, but compliance was not verified. On average, patients wore their TLSOs for 26 months (range, 7 to 50 months). After an average of 41 months of follow-up (range, 24 to 119 months), the average Cobb angle was 341.7 degrees. The six degrees of coronal plane progression was statistically significant by a matched pairs t test (p.001). From cephalad to caudad vertebrae, the concave-to-convex height ratios were: 0.900.01, 0.870.01 and 0.910.01. These concave-to-convex height ratios were not significantly different from the initial height measurement ratios (p.65). The initial Cobb measurements and concave-to-convex height ratios between Group A and Group B were equivalent (Table 3). When the brace was applied, Group B had a statistically significantly greater improvement in the Cobb measurement (65% versus 33%; p.0001). Group B also demonstrated a statistically significant radiographic improvement in the concave-to-convex height ratio when the brace was applied (p.0001; Table 4). At final follow-up, Group B patients demonstrated statistically significant improvements in their concave-to-convex height ratios (p.0001) without a significant change in the Cobb measurement. Group A patients, however, demonstrated statistically significant worsening in the Cobb measurement (p.024) without significant progression in the concave-toconvex height ratios (p.34). Discussion Numerous studies have documented the immediate and long-term benefits of brace treatment on Cobb measure-

Table 2 Sequential measurements of vertebral body wedging

Group A Group B Initial Cobb In brace Cobb Final Cobb

King I 5 3 King II 16 9 King III 11 5 King IV 4 2 King V 5 2 Total 41 21

2 7 6 2 3 20

27 30 26 33 24 27  0.9

10 19 11 9 12 14  1.3*

Sex: 38 females, 3 males Average age 12.1 years old Average follow-up: 41 months (range 24 to 119 months) Average number of months in brace: 26 (range 7 to 50) *In brace versus initial Cobb; a paired t test (p.0001). † Final versus initial Cobb; a paired t test (p.001).

29 35 34 34 34 34  1.7†

Vertebral body (n  41) Above apex At apex

Apical three vertebral bodies Below apex (n  123)

Initial measurement 0.91  0.01 0.85  0.01 0.91  0.01 0.89  0.01 Brace measuremetn 0.93  0.01 0.88  0.01 0.92  0.01 0.91  0.01* Final measurement 0.91  0.01 0.87  0.01 0.91  0.01 0.89  0.01† *p.0035 when the initial out-of-brace concave-to-convex height ration was compared with the in-brace concave-to-convex height ratio by a matched pairs t test. † Matched pairs comparison of initial versus final concave-to-convex height ratios (p.65).

F.P. Castro et al. / The Spine Journal 3 (2003) 180–185 Table 3 Retrospective comparison of patients with adolescent idiopathic scoliosis with and waithout radiographic progression Group A Group B

n

Initial Cobb

In-brace Cobb

Final Cobb

21 20

27 29

18* 10*

41† 27*

A matched pairs t test was used for all comparisons against the initial Cobb measurement.

ments in patients with AIS [3–6,8–11]. The initial 50% reduction and the final 20% increased average Cobb measurements seen in this study were consistent with those reports. In order to determine the positional effect that brace application had on the apical three vertebral bodies, the interval between the initial radiograph and the radiograph in a brace was 6 weeks or less. Thus, the observed improvements in the Cobb measurements and concave-to-convex height ratios, when the brace was initially applied, were attributed to positional changes of the vertebral bodies rather than asymmetric chondrogenesis. Thoracic vertebrae, in subjects without scoliosis, are normally wedged in the sagittal plane. The ratio of anterior-toposterior heights have been reported to be between 0.83 and 0.85 for the seventh through ninth vertebral bodies [35]. The “normal” wedging of the thoracic vertebrae allow for a normal thoracic kyphosis of approximately 40 degrees [36]. Transposition of a normal spine’s thoracic kyphosis into a sagittal scoliosis has been demonstrated [37] and underlies the null hypothesis in this study. That hypothesis was that the vertebral bodies were abnormally positioned normal vertebrae. The initial concave-to-convex height ratio averages in our sample of patients with AIS was 0.85 for the apical vertebra and 0.91 for the vertebrae above and below the curve apex. The immediate return toward the “normal” concave-to-convex height ratio of 1.0 from the “normal” sagittal anterior-to-posterior height ratio of approximately 0.84 was attributed to vertebral body rotation. The initial versus final radiographic comparisons provided information on structural remodeling or rotational changes that growth and brace treatment may have induced. When the 41 patients were prospectively analyzed, no conclusions about the Hueter-Volkmann principle or structural remodeling could be reached. The ambiguity of the prospective analysis was attributed to the equivalent number of patients who demonstrated either a relative stimulation (20 pa-

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tients) or inhibition (21 patients) of the concave side of the vertebral body compared with the convex side. When the patients with AIS were retrospectively divided into Group A (radiographic progression) and Group B (no radiographic progression), several interesting conclusions were made. At least three variables were responsible for the positional improvements in concave-to-convex height ratios translating into structural improvements for Group B patients. The first variable was curve flexibility. Some believe that curve flexibility may be a much stronger predictor of successful brace treatment than the curve’s Cobb measurement [38,39]. Curve flexibility allowed for a significant initial derotation of the scoliotic deformity. These positional changes were then maintained by brace treatment. Flexible curves may have also allowed TLSO-applied distractive forces of sufficient magnitude to stimulate asymmetric chondrogensis on the concave sides of the vertebral bodies. Fifteen of 20 Group B patients demonstrated radiographic improvements in the concave-to-convex ratios of the apical vertebral body at final follow-up. More importantly, 8 of 21 patients with radiographic worsening of the Cobb measurement demonstrated radiographic improvement in the concave-to-convex height ratios of the apical vertebral body. As brace-wear compliance and brace-strap tension were not documented, another explanation for the structural remodeling of the vertebral bodies may be a higher rate of spontaneous correction in patients with AIS with flexible curves. Lonstein and Carlson [40] reported spontaneous regression of scoliotic deformities in 11% of patients with AIS observed without brace treatment. The second variable contributing to the structural remodeling of the apical three vertebral bodies was the application of the brace. TLSOs, like Harrington instrumentation, vertically distract the spine [6]. The corrective forces applied to Group B patients allowed for statistically significant immediate improvements in Cobb measurements and concave-toconvex height ratios. The initial correction seen in Group A patients was of similar direction but of insufficient magnitude compared with that seen in Group B patients. Cobb measurement worsening in Group A patients was attributed to vertebral body rotation toward the “normal” sagittal plane height ratio of 0.85. Dysfunctional endochondral ossification (a relative inhibition of the concave side) that did not respond to the distractive forces of the brace may have occurred. Thirteen of 21 Group A patients demonstrated radiographic worsening of the Cobb measurement and concave-

Table 4 Sequential measurements of vertebral body wedging Apical three vertebral bodies Brace

Final

Group

Initial measurement

Measurement

p value

Measurement

p value

Group A (radiographic progression 5 degrees) Group B (no radiographic progression)

0.88  0.01 0.90  0.01

0.91  0.01 0.93  0.01

.45* .0049

0.86  0.01 0.93  0.01

.34 .0099

*All intragroup comparisons compared the initial concave-to-convex height ratio by a matched pairs t test.

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to-convex height ratios at final follow-up. The observed results could also be explained if a higher rate of noncompliance existed in patients with AIS with rigid curves. The third variable was time in the brace or timing of the brace treatment. In order for the Hueter-Volkmann principle to be applicable, the epiphyses needed to be open and possess a significant growth potential. The discs, ligaments and other supporting soft tissues also needed to be pliable. This investigation used the Risser sign as an indicator of skeletal immaturity. Again, peak height velocity may have been a better indicator as to when brace application would be most effective [24]. Progression of the scoliotic deformity usually worsens the most during the adolescent growth spurt. Paradoxically, the adolescent growth spurt may also be the time when maximal curve correction may be induced. Patients with AIS who demonstrated radiographic progression in the current study (Group A) had less than 34% correction of their initial Cobb measurement when the TLSO was applied. Patients with AIS who progressed 15 or more degrees exhibited 20% or less correction with the TLSO applied. We therefore question the efficacy of brace treatment in patients with AIS whose Cobb measurement does not improve at least 20% of its initial value when a TLSO is applied. Given the time, effort and expense of obtaining a TLSO, perhaps a lateral side bending film, to determine curve flexibility, may be prudent. It appears that the vertebral bodies in patients with AIS were abnormally positioned but structurally and functionally normal. Successful brace treatment has been positively correlated with the total number of brace-wear hours per day [8–11]. Successful brace treatment may now also be positively correlated with the ability of the brace to initiate significant positional changes. Distractive forces may stimulate asymmetric chondrogenesis when patients are supine and prevent dysfunctional chondrogenesis when patients are standing, but this was difficult to prove. Nighttime only and nighttime weaning out of the TLSO are predicated on the assumption that the distractive forces of the brace work even when the patient is supine [10,41]. Brace-induced, softtissue-mediated rotations of the vertebral bodies probably best explain the effect of brace treatment on AIS curves. Measurement error, as well as the lack of documented brace wear, may represent weaknesses of the study. Vertebral body rotation is notoriously inaccurate on unidimensional radiographs. A measuring error of 1 mm may significantly change a concave-to-convex height ratio. Similarly, the radiographs on which the results were based ignore the threedimensional deformity of scoliotic curves. Larger cohorts with spiral computed tomographs may someday elucidate whether the Hueter-Volkmann principle and vertebral body remodeling (if any) occur in brace-treated patients with AIS. In conclusion, the retrospective analysis of the data, compared with the prospective analysis, was more insightful in determining the importance of curve flexibility as a predictor of successful brace outcome. Brace application was a successful treatment when the initial vertebral body derota-

tions were maintained until skeletal maturity. The efficacy of brace treatment in patients with rigid curves was questioned. A side-bending radiograph to assess curve flexibility may be cost effective in preventing TLSO application to patients, with rigid curves, unlikely to benefit from its use. Acknowledgments The author would like to thank Drs. Amy Young, James Bennett, Corey Solman, and Dennis DeVito for their help during the investigation. References [1] Dickson RA, Weinstein SL. Bracing (and screening)—yes or no? J Bone Joint Surg Br 1999;81B:193–8. [2] Fernandez-Feliberti R, Flynn J, Ramirez N, Trautmann M, Alegria M. Effectiveness of TLSO bracing in the conservative treatment of idiopathic scoliosis. J Pediatr Orthop 1995;15(2):176–81. [3] Lonstein JE, Winter RB. The Milwaukee brace for the treatment of adolescent idiopathic scoliosis. A review of one thousand and twenty patients. J Bone Joint Surg 1994;76A(8):1207–21. [4] Nachemson AL, Peterson LE. Effectiveness of treatment with a brace in girls who have adolescent idiopathic scoliosis. A prospective, controlled study based on data from the Brace Study of the Scoliosis Research Society. J Bone Joint Surg 1995;77A(6):815–22. [5] Korovessis P, Kyrkos C, Piperos G, Soucacos PN. Effects of thoracolumbosacral orthosis on spinal deformities, trunk asymmetry, and frontal lower rib cage in adolescent idiopathic scoliosis. Spine 2000; 25(16):2064–71. [6] Labelle H, Dansereau J, Bellefleur C, Poitras B. Three-dimensional effect of the Boston brace on the thoracic spine and rib cage. Spine 1996;21(1):59–64. [7] Lonstein J. Scoliosis. In: Morrissy RT, Weinstein SL, editors. Scoliosis in Lovell and Winter’s pediatric orthopaedics, vol. 2, 4th ed. Philadelphia, PA: Lippincott-Raven, 1996:648. [8] Rowe DE, Bernstein SM, Riddick MF, Adler F, Emans JB, GardnerBonneau D. A meta-analysis of the efficacy of non-operative treatments for idiopathic scoliosis. J Bone Joint Surg 1997;79A:664–74. [9] Green NE. Part-time bracing of adolescent idiopathic scoliosis. J Bone Joint Surg 1986;68A:738–42. [10] Price CT, Scott DS, Reed F Jr, Sproul JT, Riddick MF. Nighttime bracing for adolescent idiopathic scoliosis with the Charleston bending brace: long-term follow-up. J Pediatric Orthop 1997;17(6):703–7. [11] Howard A, Wright JG, Hedden D. A comparative study of TLSO, Charleston, and Milwaukee braces for idiopathic scoliosis. Spine 1998;23(22):2404–11. [12] Aubin C-E, Labelle H, Ruszkowski A, et al. Variability of strap tension in brace treatment for adolescent idiopathic scoliosis. Spine 1999;24(4):349–54. [13] Yamada K, Yamamoto H, Nakagawa Y, Tezuka A, Tamura T, Kawata S. Etiology of idiopathic scoliosis. Clin Orthop 1984;184:50–7. [14] Kindsfater K, Lowe T, Lawellin D, Weinstein D, Akmakjian J. Levels of platelet calmodulin for the progression and severity of adolescent idiopathic scoliosis. J Bone Joint Surg 1994;76A:1186–92. [15] Machida M. Cause of idiopathic scoliosis. Spine 1999;24(24):2576–83. [16] Goldberg CJ, Dowling FE, Hall JE, Emans JB. A statistical comparison between natural history of idiopathic scoliosis and brace treatment in skeletally immature adolescent girls. Spine 1993;18(7):902–8. [17] Dickson RA, Lawton JO, Archer IA, Butt WP. The pathogenesis of idiopathic scoliosis biplanar spinal asymmetry. J Bone Joint Surg Br 1984;66B:8–15. [18] McCarroll HR, Costen W. Attempted treatment of scoliosis by unilateral vertebral epiphyseal arrest. J Bone Joint Surg 1960;42A:965–78.

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